ECOHYDROLOGY
Ecohydrol. (2015)
Published online in Wiley Online Library
(wileyonlinelibrary.com) DOI: 10.1002/eco.1601
Proximity to encroaching coconut palm limits native forest
water use and persistence on a Pacific atoll
Ken W. Krauss,1 Jamie A. Duberstein,2* Nicole Cormier,1 Hillary S. Young3 and
Stacie A. Hathaway4
1
US Geological Survey, National Wetlands Research Center, 700 Cajundome Blvd., Lafayette, LA, 70506, USA
Baruch Institute of Coastal Ecology and Forest Science, Clemson University, Georgetown, SC, 28442, USA
Department of Ecology, Evolution and Marine Biology, University of California – Santa Barbara, Noble Hall 2116, Santa Barbara, CA, 93106-9620,
USA
4
US Geological Survey, Western Ecological Research Center, 4165 Spruance Road, Suite 200, San Diego, CA, 92101, USA
2
3
ABSTRACT
Competition for fresh water between native and introduced plants is one important challenge facing native forests as rainfall
variability increases. Competition can be especially acute for vegetation on Pacific atolls, which depend upon consistent rainfall
to replenish shallow groundwater stores. Patterns of sap flow, water use, and diameter growth of Pisonia grandis trees were
investigated on Sand Islet, Palmyra Atoll, Line Islands, during a period of low rainfall. Sap flow in the outer sapwood was
reduced by 53% for P. grandis trees growing within coconut palm (Cocos nucifera) stands (n = 9) versus away from coconut
palm (n = 9). This suggested that water uptake was being limited by coconut palm. Radial patterns of sap flow into the sapwood
of P. grandis also differed between stands with and without coconut palm, such that individual tree water use for P. grandis
ranged from 14 to 67 L day1, averaging 47·8 L day1 without coconut palm and 23·6 L day1 with coconut palm. Diameter
growth of P. grandis was measured from nine islets. In contrast to sap flow, competition with coconut palm increased diameter
growth by 89%, equating to an individual tree basal area increment of 5·4 versus 10·3 mm2 day1. Greater diameter growth
countered by lower rates of water use by P. grandis trees growing in competition with coconut palm suggests that stem swell
may be associated with water storage when positioned in the understory of coconut palm, and may facilitate survival when water
becomes limiting until too much shading overwhelms P. grandis. Copyright © 2015 John Wiley & Sons, Ltd.
KEY WORDS
dendrometry; invasion biology; sap flow; scaling; tree water use; Palmyra Atoll; Pacific islands
Received 27 June 2014; Revised 12 December 2014; Accepted 24 December 2014
INTRODUCTION
The majority of the world’s atoll environments occur in the
Pacific Ocean. Pacific atolls are often forested with endemic
plant assemblages that provide critically unique nesting
habitat for seabirds (King, 1973; Walker, 1991). Among
these endemic communities are Pisonia grandis R. Br.
forests (hereafter, Pisonia forests), which typically form on
coralline substrates and produce underlying humic peat soils
over successive years (Fosberg, 1957). These forests are
becoming increasingly imperilled because of agricultural
land clearing (Fosberg, 1983), insect invasions (Handler
et al., 2007), reduced nutrient subsidies (Greenslade, 2008;
Young et al., 2010), and direct competition with coconut
palm (Cocos nucifera L.) (Hathaway et al., 2011). Thus,
Pisonia forest decline has been exacerbated by present and
*Correspondence to: Jamie A. Duberstein, Baruch Institute of Coastal
Ecology and Forest Science, Clemson University, Georgetown, SC 28442,
USA.
E-mail: [email protected]
Copyright © 2015 John Wiley & Sons, Ltd.
past land use activities; among these have been the
widespread proliferation of coconut palm plantations
throughout Micronesia (Mueller-Dombois and Fosberg,
1998). Efforts to protect Pisonia forests as critical habitat
throughout the Pacific mandate a comprehensive understanding of the competition afforded by coconut palm.
While Pisonia forests occur throughout the Indo-Pacific
region (Airy Shaw, 1952; Mueller-Dombois and Fosberg,
1998), we focus on Palmyra Atoll which, because of its
protected status as a National Wildlife Refuge of the United
States, represents some of the most intact remaining Pisonia
forests in the world (Hathaway et al., 2011). Pisonia forests
on Palmyra Atoll receive large inputs of nutrient subsidies in
the form of guano deposited from nesting seabirds, but
subsidies are disrupted when suitable nesting trees are
supplanted by coconut palm (Young et al., 2010). Nesting
seabirds have a strong preference for native P. grandis or
Tournefortia argentea L. f. trees over coconut palm (Young
et al., 2010). This creates feedbacks for regeneration, as P.
grandis and T. argentea have much higher growth and
establishment rates when receiving nutrient subsidies,
K. W. KRAUSS et al.
whereas coconut palm seedlings experience no growth
benefit (Young et al., 2011). However, while these
differences in nutrient gradients may explain trends towards
monodominance of coconut palm once established, they do
not fully explain how and why coconut palms encroach into
P. grandis habitat over time. Consideration must thus be
given to other factors stressing mature P. grandis when they
are in allopatric associations with coconut palm.
Indeed, the causes of Pisonia forest demise are not
straightforward. On the one hand, defoliation and perhaps
even mortality of Pisonia forests may be punctuated by
specific environmental conditions (Greenslade, 2008).
Widespread defoliation of P. grandis trees on Palmyra
Atoll was detected in 2001, and between 2002 and 2005
there was a loss of approximately 34% of P. grandis trees
(Hathaway et al., 2011). Handler et al. (2007) noted that
the green scale insect Pulvinaria urbicola Cockerell was
particularly abundant on trees of poor health, and revealed
a mutualistic relationship between introduced bigheaded
ants (Pheidole megacephala Fabricius) and the scale insect.
This mutualism between introduced scale and ant communities was implicated in fostering higher population levels
of both, causing defoliation of P. grandis trees on Palmyra
Atoll (Handler et al., 2007) and in other Pisonia forests
worldwide (Batianoff et al., 2010). On the other hand,
the mechanisms driving these outbreaks spatially as well
as other types of stress within Pisonia forests are cryptic
though not mutually exclusive. We suspect that reduced
tree health and vigour may originate as secondary stress
effects to Pisonia forests, especially during lower
rainfall years (Greenslade, 2008; McDowell et al.,
2008), and may be punctuated by direct competition
between P. grandis and coconut palm for freshwater
resources.
Palmyra Atoll is situated five degrees above the equator
and considered a wet atoll with average reported rainfall
over 4000 mm year1 (Mueller-Dombois and Fosberg,
1998). However, rainfall can be low in some years, such
as 2011 and 2012 (this study) when annual rainfall totalled
3197 and 2851 mm, respectively. Lower rainfall over
specific weeks might foster reduced soil hydration within
the root zone and force water extraction from a limited
freshwater lens beneath soils during those times (Meehl,
1996). Groundwater is a critical source of fresh water to
atoll vegetation (Urish, 1974). A freshwater lens is a layer
of non-saline groundwater situated above saline water, is
typically deeper on the lagoon side, and is subject to tidal
and climatic fluctuations (Urish, 1974). Coconut palm
proliferates atop freshwater lenses throughout the Pacific.
Yet, coconut palm is not native to the atoll (Maloney,
1993) but was established on Palmyra by 1927
(Christophersen, 1927). Because coconut palm uses a
considerable amount of water (30–120 L day1: Jayasekara
and Jayasekara, 1993; 93–160 L day1: Roupsard et al.,
Copyright © 2015 John Wiley & Sons, Ltd.
2006) and has a drought-tolerant physiology (e.g., high
membrane stability, etc.: Gomes and Prado, 2007), coconut
palm probably competes favourably with P. grandis for
available water. Both species have shallow root systems
adapted to use fresh water near the soil surface while
avoiding contact with saline water (Walker, 1991; Gomes
and Prado, 2007), but the efficiency with which either
species relies on rainfall replenishment, antecedent rain
water within shallow water tables, or deeper groundwater
stores during drier periods is unclear. Both P. grandis and
coconut palms are able to retain fresh water via storage in the
main stem, but Gomes and Prado (2007) posit that the rate of
water uptake may be rapid in coconut palms following rain
events.
After investigating several nutrient and biotic influences
on P. grandis forest dynamics on Palmyra (Young et al.,
2010; Young et al., 2011; Young et al., 2013), we suggest
that competition for water resources between P. grandis
and coconut palm on Palmyra Atoll, and perhaps other
atolls throughout the Pacific, is likely a major contributor to
the overall reduced health of Pisonia forests. The health of
Pisonia forests is central to atoll management (Hathaway
et al., 2011); manually removing coconut palm will be
energy-intensive and costly, so determining whether
Pisonia forests perform better physiologically in the
absence of coconut palm was central to our investigation.
We hypothesized that P. grandis trees would have lower
rates of water use and growth in forest stands in which
coconut palms were intermixed.
METHODS
Study sites
Palmyra Atoll contains tropical wet forests situated at the
northern end of the Line Island chain in the equatorial
Pacific Ocean (Figure 1: 162°05′W, 5°53′N). The atoll was
altered dramatically during the US military occupation
(1940–1945); some areas were dredged and others filled,
resulting in a mixture of natural and constructed islets
(Collen et al., 2009). Impacts to vegetation on all islets
were substantial during the military occupation, equating to
complete ecesis in many cases even among natural islets.
The volume of land above sea level on Palmyra Atoll
increased threefold during the military occupation (Collen
et al., 2009).
Two predominant forest types occur on Palmyra Atoll:
(1) interior stands of P. grandis with fringing T. argentea,
and (2) coconut palm communities (Young et al., 2011).
These forest types do intermix in many locations. We
established two primary study sites on Sand Islet from
which sap flow and diameter growth studies were initiated.
This islet was created in the 1940s entirely from dredge
material and thus has very uniform substrate and elevation.
Ecohydrol. (2015)
WATER USE STRATEGIES OF NATIVE TREES ON ATOLLS
Figure 1. Aerial view of Palmyra Atoll and the associated islets from which sap flow and diameter studies were conducted. Sample sizes (n) of trees for
diameter studies, P. grandis stand association with and without coconut palm, and location of the weather station are depicted.
Likely due in part to its location on the far western edge of
the atoll, Sand Islet also has very high densities of nesting
seabirds and thus consistently high nitrogen and phosphorus levels across the islet (~1 SD above mean from all other
islets; Young et al., 2010; H.S. Young, unpubl.). We thus
expect that nutrient limitation is minimal across this islet.
Beyond these two focal sites, ten additional study sites
were located at various islets across the atoll to encompass
a broader range of conditions from which only diameter
growth studies were initiated. Sites were established on a
variety of islets representing two P. grandis forest stand
associations: P. grandis growing away from coconut palm
(n = 6, ‘without palm’) and P. grandis growing in
association with coconut palm (n = 6, ‘with palm’)
(Figure 2). T. argentea was often associated with P.
grandis, but P. grandis trees had to be at least 6 m from the
nearest coconut palm to be categorized as occurring
‘without palm’. Distances were often much greater.
Diameter at breast height (dbh) of P. grandis trees (banded,
see Diameter Growth below) averaged 34·3 ± 1·8 SE cm on
sites without palm and 34·0 ± 2·3 SE cm on sites with palm;
we were careful to match tree size. Average P. grandis tree
height ranged from 10·6–16·7 m among all stands.
Sap flow measurements
Sap flow measurements were made on P. grandis trees on
Sand Islet in the two stand associations (without palm, with
palm). Stand basal area ranged from 55·1–56·7 m2 ha1
(Table I), and the basal area distribution among species in
each plot on Sand Islet was fairly representative of all
Pisonia forests without palm (P. grandis > 70% basal area
versus T. argentea) and with palm (P. grandis ~50% basal
area versus C. nucifera) surveyed on Palmyra Atoll. Sand
Copyright © 2015 John Wiley & Sons, Ltd.
Figure 2. Examples of (A) P. grandis trees growing in relative
monospecific stands without coconut palm (‘without palm’) on Sand
Islet, and (B) P. grandis trees growing in association with coconut palm
(‘with palm’) on Whippoorwill Islet, Palmyra Atoll. Image credits: US
Geological Survey, K.W. Krauss (photographer).
Islet is composed of homogeneous, essentially identical
dredge material at the same water level, allowing us to
standardize local environmental conditions for sap flow
measurements while limiting the distance between the two
stands to <75 m (Figure 1).
Ecohydrol. (2015)
K. W. KRAUSS et al.
Table I. Forest structure of stands on Sand Islet, Palmyra Atoll used to measure sap flow in co-dominant P. grandis trees.
Data were collected from 0·05 ha circular plots.
P. grandis stand association
Without palm
With palm
Species
Basal area (m2 ha1)
% of plot
Pisonia grandis
Tournefortia argentea
Total
Pisonia grandis
Cocos nucifera
Total
39·69
16·95
56·65
29·28
25·78
55·06
70%
30%
We used heat dissipation sap probes (Granier, 1987)
configured to measure sap flow (g H2O m2 sapwood s1) at
radial sapwood depths of 5, 15, 25, 50, 70, and 90 mm
(TDP10-100, FLGS-TDPXM1000, Dynamax, Inc., TX,
USA). Heat dissipation sap probes have wide application for
determining individual tree water use characteristics, and
their construction requirements, formulation, and assumptions are well described (Granier, 1987; Smith and Allen,
1996; Lu et al., 2004; references therein). Furthermore,
appropriate applications for the use of multi-depth sap
probes to scale sap flow measurements to individual tree
water use have also been described (James et al., 2002; Ford
et al., 2004; Krauss and Duberstein, 2010).
We inserted paired sap probes (4 cm apart) to multiple
depths (10–90 mm) into P. grandis trees at breast height
(~1·4 m above ground); depths were associated with active
sapwood bands in co-dominant trees. Sap probes measure
temperature differences across embedded thermocouples
between heated and unheated probe pairs. These
measurements were used to calculate sap flow at the
location of the thermocouple junction and assumed to be
representative of flow over 1–2 cm lengths (but see
Clearwater et al., 1999). Probes are heated by several
deep-cycle, 12-V batteries routing power to the probes
through voltage regulators. Sap flowing over the heated
probe cools the probe according to the properties of wood
and water (Granier, 1987), such that greater sap flow cools
the heated probe to temperatures nearer that of the unheated
probe. The temperature differentials between the heated
and unheated probes are converted to water flux rates
relative to overnight and early-morning (Midnight – 0500)
no-flow conditions (sensu Oishi et al., 2008) through
established formulas (Granier, 1987). Sap flow data were
recorded every 30 min and stored in a datalogger (CR1000,
Campbell Scientific, Logan, UT, USA). On each Sand Islet
P. grandis stand association (without palm, with palm),
nine co-dominant P. grandis trees were measured, with
some trees having multiple probes at different sapwood
depths as follows: 5 (n = 2), 15 (n = 9), 25 (n = 2), 50 (n = 1),
70 (n = 3), and 90 mm (n = 1). Thus a total of 18 trees across
two stands were measured for sap flow over 34 days from
24 August to 27 September 2011.
Copyright © 2015 John Wiley & Sons, Ltd.
53%
47%
Tree water use
Water use was estimated from the outer sapwood
(0–90 mm) for each tree (n = 18) instrumented with sap
probes. Individual tree water use (in L) on a per-second
basis was determined according to the following formula:
n
Jsi
Individual tree water use ¼ ∑ Js15mm SAi Js15mm
i¼1
(1)
where i is radial depth into the sapwood, 1 is the first depth
into the sapwood, Js15mm is the stand-specific maximum
average measured rate of sap flow (see MSR below) at a
radial depth of 15 mm, SAi is the cross-sectional individual
tree sapwood area of the conductive tissue measured by
the heating probe at the ith depth, and the function Jsi/
Js15mm describes the attenuation of sap flow with radial
depth into the tree relative to sap flow at 15 mm. Jsi/Js15mm
was established separately for each P. grandis stand
association and applied to all trees in that association.
Individual tree water use (g H2O second1) was modeled
through a series of steps. Area of sapwood for each tree
(derived from dbh measurements) was first multiplied by
the pertinent attenuation function, then summed across all
cross-sectional areas of that tree. P. grandis trees in both
stand associations had maximum average sap flow rates on
17 September 2011, which we use as the Maximum
Standard Rate (MSR) of sap flow, computed independently for the two stands; this corresponded to clear
atmospheric conditions. Whole-tree sap flow rates on a
per-second basis were summed to 30-min periods, then
scaled independently (for each tree) by multiplying by a
diurnal adjustment factor. The diurnal adjustment factor
was calculated as percent of sap flow occurring for each
30-min period at MSR. The adjusted rates (now reflecting
maximum rates per tree) were then converted to daily
rates (kg or L H2O day1) by summing across all
(adjusted) 30-min intervals for each day. Cumulative
daily values for vapour pressure deficit (D) were used to
scale individual tree water use among days (n = 35 days);
e.g., if cumulative D for 24 August was 68% of
cumulative D occurring during MSR (17 September for
Ecohydrol. (2015)
WATER USE STRATEGIES OF NATIVE TREES ON ATOLLS
this study), then water use by all trees would also be
68% of MSR in our calculations for that day. We assume
that daily cumulative D accounts for alterations in
individual tree water use of dominant trees caused by
normal weather patterns, including rainfall, cloud cover,
and temperature fluctuations. Sap flow at radial depths
>90 mm were not measured and were excluded by these
procedures (see Discussion section).
Diameter growth
Pisonia forests with and without coconut palms were
selected on nine Palmyra Atoll islets, including Sand,
Holei, Portsmouth, Eastern, Leslie, Paradise, Kaula,
Whippoorwill, and Strawn (Figure 1). Non-vernier,
stainless steel dendrometer bands were installed at
approximate dbh (or accepted deviations, Avery and
Burkhart, 1994) using established protocols (Cattelino
et al., 1986). Trees were scraped lightly with a rasp to
ensure a tight fit by removing loose bark, and bands were
installed tightly around the circumference of each tree.
Non-corroding springs were used to keep bands tight
during circumference expansion or retraction, which was
recorded relative to etchings made on the band during
installation. Circumference increment (±) was recorded to
the nearest 0·25 mm and converted to individual tree basal
area increment using initial dbh values (Krauss et al.,
2007a). In each stand, eight to ten trees were typically
banded (but two stands had six trees; Figure 1), for a total
of 106 trees. Trees were measured three times over
approximately 663 days from 23 September 2010 to 17
July 2012, with slight date variations among individual
stands.
Environmental measurements
We installed a weather station on Cooper Islet in an open
area approximately 2·5 km from Sand Islet (Figure 1). Air
temperature and relative humidity were measured with a
combination probe inserted into a vented radiation shield
(Vaisala, Model HMP45C, Vaisala Oyj, Helsinki, Finland),
and photosynthetically active radiation (PAR) was measured
with a base-levelled quantum sensor (LI-190SA, Li-Cor
Environmental, Lincoln, NE, USA). Sensors were connected
to a datalogger (CR800, Campbell Scientific, Inc., Logan,
UT, USA) powered by an internal battery and solar panel,
and programmed to record average response at 15-min
intervals. Rainfall was recorded using a tipping bucket rain
gauge (Model 380C, Met One Instruments, Inc., Grants
Pass, OR, USA). Two small, self-contained temperature and
relative humidity sensors were installed at the base of the
live P. grandis canopy (~8–10 m) on each Sand Islet sap
flow study plot (HOBO Pro v. 2, Onset Computer Corp.,
Bourne, MA, USA) and set to record at 30-min intervals.
Temperature and relative humidity data were used to
Copyright © 2015 John Wiley & Sons, Ltd.
calculate vapour pressure deficit (D) from open and subcanopy positions.
Statistical analyses
All statistical tests were conducted at an alpha of 0·05 using
SAS version 9·3 (SAS Institute, Cary, NC, USA). Model
residuals were either normally distributed or transformed.
Variance structures differed by analysis and were
accounted for appropriately.
Sap flow data collected from 15 mm sapwood depths. We
first tested for differences between P. grandis stand
associations (without palm, with palm) on the average rate
of sap flow at 15 mm radial depths for 18 P. grandis trees
(n = 9 per stand). All trees had active sap flow every day
between 10:30 and 18:30, and sap flow rates during that
period were used to compute a daily average rate of sap
flow for each tree. Because of the significant correlation
between either D or PAR and sap flow (r2 = 0·339 and
r2 = 0·341, respectively), we used daily average sap flow as
the response variable, and daily average D and PAR as
covariates in a repeated measures analysis of covariance
with an autoregressive process for correlated error. A test
for equal variances between sites was rejected (P < 0·001,
χ 2 = 121·7, d.f. = 1), so the statistical model assumed
unequal variances between stands.
Sap flow data collected from all sapwood depths. We
calculated radial sap flow attenuation for each P. grandis
stand association based on individual tree responses on
days without rain events and with strong coupling of D,
PAR, and sap flow; 11 of 34 days fit these criteria. Sap flow
at each radial depth into the sapwood was averaged specific
to individual trees for each day. We considered the sap
flow active when individual tree measurements at the
15 mm radial depth were >1 g H2O m2 sapwood s1.
Percent attenuation for each radial depth was then
computed by dividing the overall average rate of sap flow
for each radial depth by the overall average rate at 15 mm
(i.e., [average Jsi]/[average Js15mm]).
Tree water use. Individual tree water use was analyzed
with a repeated measures analysis of variance (ANOVA)
without specifying a covariate. Repeated measures using a
compound symmetry error structure were significantly
correlated (P < 0·001). A test for equal variances between
sites was rejected (P < 0·05, χ 2 = 6·23, d.f. = 2), so the
statistical model assumed unequal variances between stands.
Diameter growth and linkages to tree water use. Average
rates of individual tree (n = 6–10 trees per stand) basal area
growth increment (mm2 day1) of P. grandis trees growing
with and without coconut palms were compared over time
Ecohydrol. (2015)
K. W. KRAUSS et al.
using a repeated measures ANOVA without specifying a
covariate. Repeated measures using a compound symmetry
error structure were significantly correlated (P = 0·032). A
test for equal variances between sites was rejected
(P < 0·001, χ 2 = 127·9, d.f. = 2), so the statistical model
assumed unequal variances between stand types. Using
initial dbh values, we then applied the stand-specific
calculations of water use developed from Sand Islet to all
P. grandis trees having dendrometer bands on Palmyra
Atoll (n = 106) in order to relate daily growth of individual
trees (basal area increment, mm2 day1) to daily potential
individual tree water use (L day1) across the atoll. Outliers
(>3 SD from mean daily basal area increment or daily
water use) were removed (n = 4 trees) prior to analysis;
censoring was carried out using SigmaPlot 11·0 (Systat
Software, Inc., San Jose, CA, USA).
RESULTS
Sap flow data collected from 15 mm sapwood depths
Average sap flow at 15 mm radial depths for P. grandis
on Sand Islet was higher when trees did not associate
with coconut palm versus when they were growing near
coconut palm (Figure 3, P < 0·001, F = 37·55, d.f. = 16).
Between 10:30 and 18:30, rates of sap flow averaged
18·30 ± 0·47 (SE) g H2O m2 sapwood s1 in P. grandis
trees without palms and 8·69 ± 0·25 g H2O m2 sapwood
s1 for P. grandis trees with palms (Figure 3). Sap flow
was strongly controlled by D for all P. grandis trees in
both stand associations, which affected day-to-day
variability in sap flow and potential water use.
Sap flow data collected from all sapwood depths
Regardless of stand association, sap flow rates were low in
the outermost radial depth measured (i.e., 5 mm) relative to
flows at 15 mm, averaging roughly 20–25% of rates at
15 mm (Table II, Figure 4). At 25 mm, sap flow of P. grandis
was nearly double (1·76×) the rate at 15 mm when P. grandis
trees were associated with coconut palm. P. grandis sap flow
was reduced at 70 mm depths relative to 15 mm depths in
palm stands but increased to approximately 83% of 15 mm
flows at 90 mm. For P. grandis stand associations without
coconut palm, sap flow rates for P. grandis at 25 and 50 mm
were lower than at 15 mm, but varied from 1·22× to 0·80×
the 15 mm rate for 70 and 90 mm depths, respectively
(Figure 4).
Tree water use
Individual tree water use by P. grandis on Sand Islet was
higher when trees did not associate with coconut palm
versus stands having coconut palm (P < 0·001, F = 20·91,
d.f. = 16); average water use was 47·8 ± 4·4 versus 23·6 ± 3·0
(SE) L H2O day1 in the two stands, respectively. Individual
tree water use among the nine trees in each stand association
ranged from an average of 23–68 L H2O day1 without
coconut palm and 14–37 L H2O day1 with coconut palm;
however, sap flow likely continued beyond the maximum
radial depths assessed (90 mm) in trees in both stands.
Diameter growth and linkages to tree water use
P. grandis diameter growth differed between the two stand
associations over time (P = 0·005, F = 7·01, d.f. = 2). Over
approximately 663 days, growth rates for P. grandis trees
Figure 3. (A) Daily patterns of sap flow, (B) fluctuations in photosynthetically active radiation (PAR) and vapour pressure deficit (D) at the weather
station on Cooper Islet, and (C) daily average rates of sap flow at 15 mm radial depths for P. grandis trees (n = 18) with and without coconut palms on
Sand Islet. Note that rain events (e.g., 14 September) cause sharp decreases in D and PAR, which directly affect sap flow.
Copyright © 2015 John Wiley & Sons, Ltd.
Ecohydrol. (2015)
WATER USE STRATEGIES OF NATIVE TREES ON ATOLLS
Table II. Sap flow attenuation averages at various depths, relative to rates at the 15 mm radial depth. Attenuation (±1 SE) was based on
variation in data collected over 11 days during which smooth diurnal curves were observed, indicating lack of rainfall events. The
number of individual trees sampled for each radial depth is indicated (n).
Jsi/Js15mm
Without palm
5 mm
15 mm
25 mm
50 mm
70 mm
90 mm
With palm
Average
Standard error
n
Average
Standard error
n
0·19
1·00
0·82
0·94
1·22
0·80
0·00
—
0·04
0·01
0·01
0·01
2
9
2
1
3
1
0·25
1·00
1·76
1·16
0·58
0·83
0·01
—
0·03
0·01
0·01
0·01
2
9
2
1
3
1
without coconut palm (5·4 mm2 day1) were roughly half
those of trees in palm stands (10·3 mm2 day1; Figure 5).
Regression analysis of daily growth versus daily water use
produced insignificant slopes for each stand type, but the
pattern of water use and growth is nonetheless clear: P.
grandis trees used more water when not competing with
coconut palm but exhibit less stem growth in those same
conditions (Figure 6).
DISCUSSION
Water use by P. grandis on Palmyra Atoll
Figure 4. Average attenuation of sap flow for various depths (see Table II
for sample sizes) relative to rates measured at a radial depth of 15 mm (Jsi/
Js15mm) by P. grandis stand association. The shaded horizontal bar reflects
sapwood depths for which underlying attenuations were applied for
calculating individual tree water use by P. grandis stand association.
Figure 5. Growth rates for P. grandis trees (n = 106 trees total) on forest
plots without coconut palm (n = 6) and with coconut palm (n = 6) on the
islets of Palmyra Atoll. Repeated measures ANOVA indicated that growth
differed significantly by stand association over time (P = 0·005);
regressions indicate rates by stand type.
Copyright © 2015 John Wiley & Sons, Ltd.
Water use among P. grandis trees on Sand Islet ranged
from 14–68 L H2O day1. Water use varied by approximately 49–65% of mean values for individual trees from
day-to-day in relation to fluctuations in atmospheric D
Figure 6. Average daily water use and average daily growth of P. grandis
trees (n = 106 trees total) in six stand associations without coconut palm
(n = 49 trees) and six stand associations with coconut palm (n = 57 trees)
throughout Palmyra Atoll.
Ecohydrol. (2015)
K. W. KRAUSS et al.
(Figure 3), such that periods of higher humidity and rainfall
on Palmyra Atoll reduced overall sap flow rates in P.
grandis. A strong relationship between tree water use and
D is expected (Meinzer et al., 1995) and indicates that
Pisonia forests are probably not undergoing acute water
deficit over diel cycles either from an interrupted supply of
water to roots or from unfavourable leaf water losses when
evaporative demand is greatest. For example, leaf-level
stomatal conductance was reduced from 1000–1400 h in
Simarouba glauca DC. trees in Costa Rica as a result of
high evaporative demand, followed by stomatal recovery
>1400 h (Brodribb and Holbrook, 2004). Evaporative
demand is greatest during low rainfall periods, which we
witnessed on Palmyra Atoll. Rainfall was 140 mm over the
34-day sap flow experiment and drove D as high as 1·7 kPa
on specific days. Although 1 day registered 58 mm of
rainfall (14 September), 20 days had no rainfall or only
trace amounts (<0·8 mm).
Individual tree water use across a range of species
surveyed globally averaged 116 ± 16 (SE) L H2O day1
(Wullschleger et al., 1998). This average value is higher than
we observed for P. grandis. Thus, overall rates of individual
tree water use by P. grandis are seemingly conservative,
such as for Vouacapoua americana Aublet (49 cm dbh, 29 L
H2O day1) and Carapa procera DC. (38 cm dbh, 52 L H2O
day1) in French Guiana (Granier et al., 1996). Indeed,
water use by P. grandis in competition with coconut palm
compares with what has been documented in salt-tolerant
tropical vegetation such as mangroves, where moderately
sized mangrove trees (5–35 cm dbh) have a very low water
use requirement in slightly hypersaline settings (<30 L H2O
day1: Krauss et al., 2007b). P. grandis trees seem to be
very well adapted to atolls in terms of their water use
requirement, especially because atolls often have shallow
groundwater lenses with unpredictable water supplies
(Urish, 1974).
However, our P. grandis water use estimates would
inherently underestimate what the trees actually use. Radial
depth measurements stopped at 90 mm; at that sapwood depth
water use was still 80–83% of flow at 15 mm (Figure 4). Sap
flow has been found as deep as 240 mm in two rather large
Anacardium excelsum (Bentero & Balb. Ex Kunth) Skeels
(98 cm dbh) and Ficus insipida Willd. (65 cm dbh) trees in
Panama (James et al., 2002). By including deeper sapwood
contributions, we would certainly increase individual tree
water use estimation. However, our best estimates suggest only
a slight increase in individual tree water use (9–12%) if we
extend the active sapwood depth to 140 mm (at 50% flow of
15 mm), not affecting our overall conclusions. Deeper
sapwood depths contribute less to overall water use because
of a smaller concentric sapwood area. In contrast to what we
found for P. grandis, water use is typically very low or zero at
a radial depth of 90 mm in many trees (e.g., Ford and Vose,
2007; Krauss and Duberstein, 2010; but see Ford et al., 2004)
Copyright © 2015 John Wiley & Sons, Ltd.
and considerably reduced by 40–50 mm into the sapwood
(e.g., Phillips et al., 1996; Oren et al., 1999; Pausch et al.,
2000). While not all tropical trees have the diffuse patterns
of water use into the sapwood that we discovered for
P. grandis (e.g., Becker, 1996; Krauss et al., 2007b), deeper
active sapwood depths might be more conducive to
promoting water storage within P. grandis stem tissue.
The influence of coconut palm on P. grandis water use
Coconut palms have been introduced from Southeast Asia
to over 80 countries and are now distributed among tropical
climates globally (Harries, 1978). As an introduced plant,
coconut palms are anomalous in that they are typically
welcomed as a contributor to subsistence economies and a
boon to tourism and are thus propagated widely (Ewel
et al., 1999). Such a successful introduction is bound to
have consequences for native vegetation, and we suggest
that coconut palms are affecting Pisonia forests on Palmyra
Atoll by forcing changes in water use patterns.
Water use among P. grandis trees is reduced significantly
when in proximity to healthy coconut palms. In our
calculations, we used two primary mathematical scalers.
The first scaler involved absolute sap flow differences. For
Sand Islet at a radial depth of 15 mm, sap flow of P. grandis
was maximized at 35·7 g H2O m2 sapwood s1 (mean,
18·3) when trees were growing away from coconut palm but
19·3 g H2O m2 sapwood s1 (mean, 8·7) when P. grandis
was growing with coconut palm. A handful of studies have
used sap flow as a measure of stress at the individual tree
level. These include applications to wetland forest trees
(Oren et al., 1999; Krauss et al., 2007b; Duberstein et al.,
2013) and upland trees (Wullschleger and Norby, 2001)
undergoing different environmental exposures (flooding,
CO2 enrichment, etc.) whereby sap flow was found to be a
sensitive metric of change. Likewise, sap flow was reduced
by 46–53% when P. grandis trees were pressed by
competition with coconut palm on Palmyra Atoll.
The second scaler involved sap flow attenuation with
radial depth into the sapwood (sensu James et al., 2002), as
profile disparities can affect individual tree water use
significantly (Krauss and Duberstein, 2010). However,
radial profiles varied most between P. grandis growing
with and without coconut palm at a radial depth of 25 mm,
which represents a 20–40 mm sapwood band in our
calculations. Thus P. grandis trees growing within coconut
palms transited nearly twice as much water at 25 mm than at
15 mm relative to the same depth comparison for P. grandis
growing away from coconut palms (Figure 4). However,
after accounting for the initially lower sap flow capacity
(scaler 1), P. grandis sap flow at 25 mm was only 34·0 g
H2O m2 sapwood s1 when in the presence of coconut
palm versus 29·2 g H2O m2 sapwood s1 when not. In this
case, a differing profile (scaler 2) for that one depth was not
enough to offset initially lower sap flow at 15 mm for P.
Ecohydrol. (2015)
WATER USE STRATEGIES OF NATIVE TREES ON ATOLLS
grandis in coconut palm stands, such that water use by
individual P. grandis trees mixed with coconut palm was
also less. We suspect that although coconut palm might be
fairly aggressive at using water at all times, with estimates of
30–160 L H2O day1 (Jayasekara and Jayasekara, 1993;
Roupsard et al., 2006), the influence of coconut palm on
Pisonia forests may indeed be more acute during lower
rainfall years when less fresh water is available overall.
We were able to compute potential evapotranspiration (ET)
using air temperature, relative humidity, and PAR (which we
used to estimate net radiation, Rn) data collected at the weather
station between 01 January 2011 – 21 December 2013.
Priestley-Taylor (Priestley and Taylor, 1972) calculations
revealed ET was lower for the one wetter rainfall year (2013:
1389 mm H2O year1) versus the two dry years (2011:
1495 mm H2O year1; 2012: 1430 mm H2O year1),
suggesting slightly less water loss to the atmosphere from all
components (vegetation, soil, rock, etc.) in the wetter year.
Total rainfall for the wetter year of 2013 was 3482 mm
excluding 16 days; equipment failure prevented us from
recording rainfall during two brief periods in 2013, and rainy
conditions prevailed during a 9-day period in December when
data were lost. Rainfall of 3197 and 2851 mm for 2011 and
2012, respectively, might not have been strikingly different
but created important day-to-day gaps in rainfall delivery and
mean daily precipitation (P; Table III).
The coralline structure of the atoll islets lends itself to rapid
depletion of water in the upper root zone following rain events,
likely promoting water stress despite the fact that P is nearly
double ET on an annual basis (Table III). We used our weather
station data to investigate the relationship between P and ET in
terms of daily rates of groundwater recharge (R = P ET;
Comte et al., 2014) to further the contention that root zone
water stress might occur despite high rainfall. Not surprisingly, there was greater daily R in 2013 (i.e., a more positive P
to ET balance) versus 2011 and 2012, though other metrics
were not entirely dissimilar among the three years (Table III).
Still, many P. grandis trees were exhibiting signs of stress
resembling that of water deficit in 2010–2012. This
evidence suggested to us that P. grandis may be more
water stressed in drier years, but the specific mechanisms
causing this are still uncertain and the importance of R
in the driest years (e.g., El Niño Southern Oscillation) is
in need of further study (e.g., Comte et al., 2014).
That said, coconut palms are known for their drought
tolerance, which they maintain by spreading hydroactive
vascular bundles throughout the stem to maintain diffuse
water use patterns (Roupsard et al., 2006), maintaining
physiological proficiency throughout the life of the stem
(Tomlinson, 2006), maintaining leaf tissue membrane
stability under water deficit (Gomes and Prado, 2007), and
storing large quantities of water in the stem within cell
vacuoles in lieu of intercellular space (Holbrook and
Sinclair, 1992). Water storage capacity increases with height
of the tree as tree volume increases (Holbrook and Sinclair,
1992), making height an advantage to growing in environments with variable rainfall. However, P. grandis is also well
adapted to drought, can readily shed its leaves (Greenslade,
2008) and, like coconut palm, can store moisture in its trunk
to help escape/tolerate drought stress (Ogden, 1981).
Mortality of trees might actually be related to a number of
simultaneous factors, e.g., defoliation with water deficit,
insect colonization, and salinization of groundwater lenses,
without an a priori causal agent (Batianoff et al., 2010). One
potential confounding factor was the presence of the green
scale insect P. urbicola seen on the leaves of many P.
grandis trees on Sand Islet immediately prior to defoliation
events. Although the P. grandis trees in our study were not
stressed to the point of defoliation, the functional capacity of
these trees for photosynthesis, water use, and growth may
have been reduced. On Palmyra, coconut palms may exert
competition for water, manifested greatest during lower
rainfall periods. However, the more acute effect that coconut
palms are likely to have on P. grandis trees relates to adding
Table III. Summary of groundwater recharge, precipitation, and evapotranspiration statistics for Palmyra Atoll for two dry years (2011
and 2012) versus one wetter year (2013).
Variable
Mean R
Min R
Max R
Days w/o rain
% year w/o rain
Total P
Total ET
Mean P
Max P
Mean P gap Length
Max P gap Length
Units
2011
2012
2013
mm day1
mm day1
mm day1
days
%
mm year1
mm year1
mm day1
mm day1
days
days
4·68
5·92
111·19
124
34·0
3197·3
1495·4
8·8
112·8
1·8
6
3·99
5·66
141·95
148
40·4
2851·3
1430·4
7·8
142·5
2·3
12
6·09
5·73
143·13
119
34·1
3482·3a
1389·4
10·0
143·5
1·8
6
R, groundwater recharge (P-ET); P, precipitation; ET, evapotranspiration.
a
Total P is excluding 16 days of data due to equipment malfunction.
Copyright © 2015 John Wiley & Sons, Ltd.
Ecohydrol. (2015)
K. W. KRAUSS et al.
progressively greater amounts of shading to influence
individual P. grandis tree survival, thereby reducing overall
photosynthetic and water use capacity at the leaf level. We
suggest that coconut palms exert both light and water
competition during low rainfall years, though our study was
not designed to test which factor is stronger.
For P. grandis on Palmyra Atoll, diameter growth
increments were greater when growing alongside coconut
palm than when growing away from coconut palm. This
result was quite opposite to individual tree water use
patterns (Figure 6), which might be explained by two
related ideas. First, P. grandis stem swell might simply be a
result of less water use by the crown during photosynthesis,
leading to greater amounts of water stored in the stem
during dry periods. In temperate forests, 5–12 L H2O day1
(or 10–22%) of daily transpiration was from water stored
in the stem (Köcher et al., 2013), whereas as much as
4–54 L H2O day1 (or 9–15%) of daily transpiration was
from water stored in the stem in some tropical trees
(Goldstein et al., 1998). Stem water reserves can be very
important to maintain as a way to ensure against future
moisture deficits (Loustau et al., 1996). The width and density
of stem parenchyma cells are quite variable from the cambium
to pith in P. grandis (Ogden, 1981), such that individual
trees might be structurally plastic to accommodate greater
stem water storage when available.
Second, P. grandis stem swell under a coconut palm
canopy may be a consequence of suppression, although not in
the classic sense that would typically give rise to diameter
reductions (Daniel et al., 1979), as we originally hypothesized. Rather, as coconut palms encroach on Pisonia forests,
this new sub-canopy position would also reduce water use
and promote greater stem hydration through reductions in D
as air temperature is reduced and relative humidity increases.
Five-month average, daytime sub-canopy D was 0·51 kPa
compared with an average D of 0·86 kPa from an open
location (weather station). Overtopping coconut palm will
presumably have a similar effect on P. grandis trees. Even at
the scale of the individual shoot, water potential in P. grandis
was 1·54 MPa when shaded and 1·77 MPa when exposed
to sunlight (Allaway et al., 1981), indicating a greater
potential to maintain turgor with some shading. Of course, the
gravest consequence would occur when shading is too high.
Implications
From a management perspective, our data suggest that
removing coconut palm may aid in conservation of critical
Pisonia forest habitats on atolls by increasing light
availability to Pisonia and reducing water stress during low
rainfall periods when fresh water is more scarce. Removing
coconut palms will increase light levels and vapour pressure
deficits and restore litterfall inputs in these forests, although it
remains unclear how this might impact competition and
Copyright © 2015 John Wiley & Sons, Ltd.
long-term successional dynamics among P. grandis and
other species. Further research on these points is needed to
effectively guide management actions. Our results may have
some implications for the management of mass mortality of
P. grandis by periodic insect defoliation. To the extent that
such infestations and associated mortality are triggered or
exacerbated by water stress, coconut removal will likely
alleviate this stress and thus may reduce vulnerability of P.
grandis. However, such defoliation seems to be pervasive in
Pisonia forests globally, even when it occurs in monocultural
stands. It thus seems highly unlikely that coconut management will be effective in preventing this threat.
ACKNOWLEDGEMENTS
We thank Diana Papoulias, Mandy Annis, Carl Orazio, and
Tom Suchanek for assistance with trip logistics, Darren
Johnson for conducting the statistical analyses, and Kevin
Lafferty for reviewing a previous draft of this manuscript.
Amanda Meyer-Pollock, James Breeden, Jerard Jardin, Ned
Brown, and Ana Miller-ter Kuile all provided valuable
support to this project. Research was funded by the USGS
Ecosystems Mission Area and USGS Climate and Land Use
Research and Development Program (salary, NC). This
work was conducted under a special use permit granted by
the US Fish and Wildlife Service (USFWS), and The Nature
Conservancy and USFWS provided critical in-kind contributions. Technical Contribution No. 6259 of the Clemson
University Experiment Station. Any use of trade, product, or
firm names is for descriptive purposes only and does not
imply endorsement by the US Government.
REFERENCES
Airy Shaw HK. 1952. On the distribution of Pisonia grandis R. Br.
(Nyctaginaceae), with special reference to Malaysia. Kew Bulletin 7:
87–97.
Allaway WG, Pitman MG, Storey R, Tyerman S. 1981. Relationships
between sap flow and water potential in woody or perennial plants
on islands of the Great Barrier Reef. Plant, Cell and Environment 4:
329–337.
Avery TE, Burkhart HE. 1994. Forest Measurements. Fourth edition,
McGraw-Hill: New York
Batianoff GN, Naylor GC, Olds JA, Fechner NA, Neldner VJ. 2010.
Climate and vegetation changes at Coringa-Herald National Nature
Reserve, Coral Sea Islands, Australia. Pacific Science 64: 73–92.
Becker P. 1996. Sap flow in Bornean heath and dipterocarp forest trees
during wet and dry periods. Tree Physiology 16: 295–299.
Brodribb TJ, Holbrook NM. 2004. Diurnal depression of leaf hydraulic
conductance in a tropical tree species. Plant, Cell and Environment 27:
820–827.
Cattelino PJ, Becker CA, Fuller LG. 1986. Construction and installation of
homemade dendrometer bands. Northern Journal of Applied Forestry 3:
73–75.
Christophersen E. 1927. Vegetation of Pacific equatorial islands. Bishop
Museum Bulletin 44: 1–79.
Clearwater MJ, Meinzer FC, Andrade JL, Goldstein G, Holbrook NM.
1999. Potential errors in measurement of non-uniform sap flow using
heat dissipation probes. Tree Physiology 19: 681–687.
Ecohydrol. (2015)
WATER USE STRATEGIES OF NATIVE TREES ON ATOLLS
Collen JD, Garton DW, Gardner JPA. 2009. Shoreline changes and
sediment redistribution at Palmyra Atoll (Equatorial Pacific Ocean):
1874–present. Journal of Coastal Research 25: 711–722.
Comte J, Join J, Banton O, Nicolini E. 2014. Modelling the response of
fresh groundwater to climate and vegetation changes in coral islands.
Hydrogeology Journal 22: 1905–1920.
Daniel TW, Helms JA, Baker FS. 1979. Principles of Silviculture. Second
edition, McGraw-Hill, New York, NY, USA.
Duberstein JA, Krauss KW, Conner WH, Bridges Jr WC, Shelburne VB.
2013. Do hummocks provide a physiological advantage to even the
most flood tolerant of tidal freshwater trees? Wetlands 33: 399–408.
Ewel JJ, O’Dowd DJ, Bergelson J, Daehler CC, D’Antonio CM, Gómez LD,
Gordon DR, Hobbs RJ, Holt A, Hopper KR, Hughes CE, LaHart M,
Leakey RRB, Lee WG, Loope LL, Lorence DH, Louda SM, Lugo AE,
McEvoy PB, Richardson DM, Vitousek PM. 1999. Deliberate
introductions of species: research needs. BioScience 49: 619–630.
Ford CR, Vose JM. 2007. Tsuga canadensis (L.) Carr. mortality will
impact hydrologic processes in southern Appalachian forest
ecosystems. Ecological Applications 17: 1156–1167.
Ford CR, McGuire MA, Mitchell RJ, Teskey RO. 2004. Assessing
variation in the radial profile of sap flux density in Pinus species and its
effect on daily water use. Tree Physiology 24: 241–249.
Fosberg FR. 1957. Description and occurrence of atoll phosphate rock in
Micronesia. American Journal of Science 255: 584–592.
Fosberg FR. 1983. The human factor in the biogeography of oceanic
islands. CR Society Biogéographie 59: 147–190.
Goldstein G, Andrade JL, Meinzer FC, Holbrook NM, Cavelier J, Jackson
P, Celis A. 1998. Stem water storage and diurnal patterns of water use in
tropical forest canopy trees. Plant, Cell and Environment 21: 397–406.
Gomes FP, Prado CHBA. 2007. Ecophysiology of coconut palm under
water stress. Brazilian Journal of Plant Physiology 19 : 377–391.
Granier A. 1987. Evaluation of transpiration in a Douglas-fir stand by
means of sap flow measurements. Tree Physiology 3: 309–320.
Granier A, Huc R, Barigah ST. 1996. Transpiration of natural rain forest
and its dependence on climatic factors. Agricultural and Forest
Meteorology 78: 19–29.
Greenslade P. 2008. Climate variability, biological control and an insect
pest outbreak on Australia’s Coral Sea islets: lessons for invertebrate
conservation. Journal of Insect Conservation 12: 333–342.
Handler AT, Gruner DS, Haines WP, Lange MW, Kaneshiro KY. 2007.
Arthropod surveys on Palmyra Atoll, Line Islands, and insights into the
decline of the native tree Pisonia grandis (Nyctaginaceae). Pacific
Science 61: 485–502.
Harries HC. 1978. The evolution, dissemination and classification of
Cocos nucifera L. Botanical Review 44: 265–319.
Hathaway SA, McEachern K, Fisher RN. 2011. Terrestrial forest
management plan for Palmyra Atoll. Open File Report 2011-1007, U.
S. Geological Survey, Reston, VA, USA.
Holbrook NM, Sinclair TR. 1992. Water balance in the arborescent palm,
Sabal palmetto. 1. Stem structure, tissue water release properties and
leaf epidermal conductance. Plant, Cell and Environment 15: 393–399.
James SA, Clearwater MJ, Meinzer FC, Goldstein G. 2002. Heat
dissipation sensors of variable length for the measurement of sap flow
in trees with deep sapwood. Tree Physiology 22 : 277–283.
Jayasekara KS, Jayasekara C. 1993. Efficiency of water use in coconut
under different soil/plant management systems. In Advances in Coconut
Research and Development, Nair MK, Khan HH, Gopalasundaran P,
Bhaskara Rao EVV (eds). Oxford & IBH Publishing: New Delhi.
King WB. 1973. Conservation status of birds of central Pacific Islands.
Wilson Bulletin 85: 89–103.
Köcher P, Horna V, Leuschner C. 2013. Stem water storage in five coexisting
temperate broad-leaved tree species: significance, temporal dynamics and
dependence on tree functional traits. Tree Physiology 33: 817–832.
Krauss KW, Duberstein JA. 2010. Sapflow and water use of freshwater
wetland trees exposed to saltwater incursion in a tidally influenced South
Carolina watershed. Canadian Journal of Forest Research 40: 525–535.
Krauss KW, Keeland BD, Allen JA, Ewel KC, Johnson DJ. 2007a. Effects
of season, rainfall, and hydrogeomorphic setting on mangrove tree
growth in Micronesia. Biotropica 39: 161–170.
Krauss KW, Young PJ, Chambers JL, Doyle TW, Twilley RR. 2007b. Sap
flow characteristics of neotropical mangroves in flooded and drained
soils. Tree Physiology 27: 775–783.
Copyright © 2015 John Wiley & Sons, Ltd.
Loustau D, Berbigier P, Roumagnac P, Arruda-Pacheco C, David JS,
Ferreira MI, Pereira JS, Tavares R. 1996. Transpiration of a 64-year-old
maritime pine stand in Portugal: 1. Seasonal course of water flux
through maritime pine. Oecologia 107: 33–42.
Lu P, Urban L, Zhao P. 2004. Granier’s thermal dissipation probe (TDP)
method for measuring sap flow in trees: theory and practice. Acta
Botanica Sinica 46: 631–646.
Maloney BK. 1993. Palaeoecology and the origin of the coconut.
GeoJournal 31: 355–362.
McDowell N, Pockman WT, Allen CD, Breshears DD, Cobb N, Kolb T,
Plaut J, Sperry J, West A, Williams DG, Yepez EA. 2008. Mechanisms
of plant survival and mortality during drought: why do some plants
survive while others succumb to drought? New Phytologist 178:
719–739.
Meehl GA. 1996. Vulnerability of freshwater resources to climate
change in the tropical Pacific region. Water, Air, and Soil Pollution
92: 203–213.
Meinzer FC, Goldstein G, Jackson P, Holbrook NM, Gutiérrez MV,
Cavelier J. 1995. Environmental and physiological regulation of
transpiration in tropical forest gap species: the influence of boundary
layer and hydraulic properties. Oecologia 101: 514–522.
Mueller-Dombois D, Fosberg FR. 1998. Vegetation of the Tropical Pacific
Islands. Springer: New York.
Ogden J. 1981. Dendrochronological studies and the determination
of tree ages in the Australian tropics. Journal of Biogeography 8:
405–420.
Oishi AC, Oren R, Stoy PC. 2008. Estimating components of forest
evapotranspiration: a footprint approach for scaling sap flux
measurements. Agricultural and Forest Meteorology 148: 1719–1732.
Oren R, Phillips N, Ewers BE, Pataki DE, Megonigal JP. 1999.
Sap-flux-scaled transpiration responses to light, vapor pressure deficit,
and leaf area reduction in a flooded Taxodium distichum forest. Tree
Physiology 19: 337–347.
Pausch RC, Grote EE, Dawson TE. 2000. Estimating water use by sugar
maple trees: considerations when using heat-pulse methods in trees with
deep functional sapwood. Tree Physiology 20: 217–227.
Phillips N, Oren R, Zimmermann R. 1996. Radial patterns of xylem sap
flow in non-, diffuse- and ring-porous tree species. Plant, Cell and
Environment 19: 983–990.
Priestley CHB, Taylor RJ. 1972. On the assessment of surface heat flux
and evaporation using large-scale parameters. Monthly Weather Review
100: 81–92.
Roupsard O, Bonnefond J, Irvine M, Berbigier P, Nouvellon Y, Dauzat J,
Taga S, Hamel O, Jourdan C, Saint-André L, Mialet-Serra I, Labouisse
J, Epron D, Joffre R, Braconnier S, Rouzière A, Navarro M, Bouillet J.
2006. Partitioning energy and evapo-transpiration above and below a
tropical palm canopy. Agricultural and Forest Meteorology 139:
252–268.
Smith DM, Allen SJ. 1996. Measurement of sap flow in plant stems.
Journal of Experimental Botany 47: 1833–1844.
Tomlinson PB. 2006. The uniqueness of palms. Botanical Journal of the
Linnean Society 151: 5–14.
Urish DW. 1974. Fresh water on the coral atoll island. The Military
Engineer 429: 25–27.
Walker TA. 1991. Pisonia islands of the Great Barrier Reef: part I. The
distribution, abundance and dispersal by seabirds of Pisonia grandis.
Atoll Research Bulletin 350: 1–23.
Wullschleger SD, Norby RJ. 2001. Sap velocity and canopy transpiration
in a sweetgum stand exposed to free-air CO2 enrichment (FACE). New
Phytologist 150: 489–498.
Wullschleger SD, Meinzer FC, Vertessy RA. 1998. A review of
whole-plant water use studies in trees. Tree Physiology 18: 499–512.
Young HS, McCauley DJ, Dirzo R. 2011. Differential responses to guano
fertilization among tropical tree species with varying functional traits.
American Journal of Botany 98: 1–8.
Young HS, McCauley DJ, Dunbar RB, Dirzo R. 2010. Plants cause
ecosystem nutrient depletion via the interruption of bird-derived spatial
subsidies. Proceedings of the National Academy of Science 107:
2072–2077.
Young HS, McCauley DJ, Guevara R, Dirzo R. 2013. Consumer
preference for seeds and seedlings of rare species impacts tree diversity
at multiple scales. Oecologia 172: 857–867.
Ecohydrol. (2015)